Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers

ABSTRACT Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among “white rot” fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates—“...

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Autores principales:	Jiwei Zhang, Kevin A. T. Silverstein, Jesus David Castaño, Melania Figueroa, Jonathan S. Schilling
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	brown rot adaption comparative transcriptomics gene regulation shift plant biomas wood-decomposing fungi Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d92cbecabb4d4c80be2389ff645756a0
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spelling	oai:doaj.org-article:d92cbecabb4d4c80be2389ff645756a02021-11-15T15:54:46ZGene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers10.1128/mBio.02176-192150-7511https://doaj.org/article/d92cbecabb4d4c80be2389ff645756a02019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02176-19https://doaj.org/toc/2150-7511ABSTRACT Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among “white rot” fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates—“brown rot.” The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene losses were due, in part, to upregulation of the retained genes. We applied comparative transcriptomics to multiple species of both rot types grown across a wood wafer to create a gradient of progressive decay and to enable tracking temporal gene expression. Dozens of “decay-stage-dependent” ortho-genes were isolated, narrowing a pool of candidate genes with time-dependent regulation unique to brown rot fungi. A broad comparison of the expression timing of CAZY families indicated a temporal regulatory shift of lignocellulose-oxidizing genes toward early stages in brown rot compared to white rot, enabling the segregation of oxidative treatment ahead of hydrolysis. These key brown rot ROS-generating genes with iron ion binding functions were isolated. Moreover, transcription energy was shifted to be invested on the retained GHs in brown rot fungi to strengthen carbohydrate conversion. Collectively, these results support the hypothesis that gene regulation shifts played a pivotal role in brown rot adaptation. IMPORTANCE Fungi dominate the turnover of wood, Earth’s largest pool of aboveground terrestrial carbon. Fungi first evolved this capacity by degrading lignin to access and hydrolyze embedded carbohydrates (white rot). Multiple lineages, however, adapted faster reactive oxygen species (ROS) pretreatments to loosen lignocellulose and selectively extract sugars (brown rot). This brown rot “shortcut” often coincided with losses (>60%) of conventional lignocellulolytic genes, implying that ROS adaptations supplanted conventional pathways. We used comparative transcriptomics to further pursue brown rot adaptations, which illuminated the clear temporal expression shift of ROS genes, as well as the shift toward synthesizing more GHs in brown rot relative to white rot. These imply that gene regulatory shifts, not simply ROS innovations, were key to brown rot fungal evolution. These results not only reveal an important biological shift among these unique fungi, but they may also illuminate a trait that restricts brown rot fungi to certain ecological niches.Jiwei ZhangKevin A. T. SilversteinJesus David CastañoMelania FigueroaJonathan S. SchillingAmerican Society for Microbiologyarticlebrown rot adaptioncomparative transcriptomicsgene regulation shiftplant biomaswood-decomposing fungiMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	brown rot adaption comparative transcriptomics gene regulation shift plant biomas wood-decomposing fungi Microbiology QR1-502
spellingShingle	brown rot adaption comparative transcriptomics gene regulation shift plant biomas wood-decomposing fungi Microbiology QR1-502 Jiwei Zhang Kevin A. T. Silverstein Jesus David Castaño Melania Figueroa Jonathan S. Schilling Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
description	ABSTRACT Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among “white rot” fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates—“brown rot.” The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene losses were due, in part, to upregulation of the retained genes. We applied comparative transcriptomics to multiple species of both rot types grown across a wood wafer to create a gradient of progressive decay and to enable tracking temporal gene expression. Dozens of “decay-stage-dependent” ortho-genes were isolated, narrowing a pool of candidate genes with time-dependent regulation unique to brown rot fungi. A broad comparison of the expression timing of CAZY families indicated a temporal regulatory shift of lignocellulose-oxidizing genes toward early stages in brown rot compared to white rot, enabling the segregation of oxidative treatment ahead of hydrolysis. These key brown rot ROS-generating genes with iron ion binding functions were isolated. Moreover, transcription energy was shifted to be invested on the retained GHs in brown rot fungi to strengthen carbohydrate conversion. Collectively, these results support the hypothesis that gene regulation shifts played a pivotal role in brown rot adaptation. IMPORTANCE Fungi dominate the turnover of wood, Earth’s largest pool of aboveground terrestrial carbon. Fungi first evolved this capacity by degrading lignin to access and hydrolyze embedded carbohydrates (white rot). Multiple lineages, however, adapted faster reactive oxygen species (ROS) pretreatments to loosen lignocellulose and selectively extract sugars (brown rot). This brown rot “shortcut” often coincided with losses (>60%) of conventional lignocellulolytic genes, implying that ROS adaptations supplanted conventional pathways. We used comparative transcriptomics to further pursue brown rot adaptations, which illuminated the clear temporal expression shift of ROS genes, as well as the shift toward synthesizing more GHs in brown rot relative to white rot. These imply that gene regulatory shifts, not simply ROS innovations, were key to brown rot fungal evolution. These results not only reveal an important biological shift among these unique fungi, but they may also illuminate a trait that restricts brown rot fungi to certain ecological niches.
format	article
author	Jiwei Zhang Kevin A. T. Silverstein Jesus David Castaño Melania Figueroa Jonathan S. Schilling
author_facet	Jiwei Zhang Kevin A. T. Silverstein Jesus David Castaño Melania Figueroa Jonathan S. Schilling
author_sort	Jiwei Zhang
title	Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
title_short	Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
title_full	Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
title_fullStr	Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
title_full_unstemmed	Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers
title_sort	gene regulation shifts shed light on fungal adaption in plant biomass decomposers
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/d92cbecabb4d4c80be2389ff645756a0
work_keys_str_mv	AT jiweizhang generegulationshiftsshedlightonfungaladaptioninplantbiomassdecomposers AT kevinatsilverstein generegulationshiftsshedlightonfungaladaptioninplantbiomassdecomposers AT jesusdavidcastano generegulationshiftsshedlightonfungaladaptioninplantbiomassdecomposers AT melaniafigueroa generegulationshiftsshedlightonfungaladaptioninplantbiomassdecomposers AT jonathansschilling generegulationshiftsshedlightonfungaladaptioninplantbiomassdecomposers
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Gene Regulation Shifts Shed Light on Fungal Adaption in Plant Biomass Decomposers

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